Vol. 83, Issue 6, 2105-2111, December 1997

Resistance training and human cervical muscle recruitment plasticity

Michael S. Conley¹, Michael H. Stone², Michael Nimmons², and Gary A. Dudley¹

¹ Department of Exercise Science, The University of Georgia, Athens, Georgia 30602; and ² Department of Health, Leisure, and Exercise Science, Appalachian State University, Boone, North Carolina 28608

ABSTRACT

INTRODUCTION

METHODS

RESULTS

DISCUSSION

ACKNOWLEDGEMENTS

FOOTNOTES

REFERENCES

ABSTRACT

Conley, Michael S., Michael H. Stone, Michael Nimmons, and Gary A. Dudley. Resistance training and human cervical muscle recruitment plasticity. J. Appl. Physiol. 83(6): 2105-2111, 1997.This study examined cervical neuromuscular adaptations to resistance training. The ResX group performed conventional resistance training plus head-extension exercise. Another group performed only conventional resistance training, and the control group performed no resistance exercise. Muscle use during head extension was determined by quantifying shifts in T2 in serial-transaxial magnetic resonance images of the neck. ResX was the only group that showed a training effect. Training decreased (P < 0.05) the cross-sectional area (CSA) of cervical muscle used to perform submaximal head extension by 31%. This reflected a decrease (P < 0.05) in relative use of the splenius capitis, semispinalis capitis, and semispinalis cervicis and multifidus muscles by about one-third; their percentage of CSA showing contrast shift was reduced from 60 to 40% on average. This same exercise evoked no contrast shift in the levator scapulae, longissimus capitis and cervicis, and scalenus medius and anterior muscles posttraining, yet 20% or more of their CSA was engaged pretraining. The relative CSA of cervical musculature that was used to perform maximal head extension was increased (P < 0.05) 16% by training. The findings suggest functional redundancy of neck musculature that can be modified by training; submaximal tasks can be performed despite cessation of recruitment of individual muscles, yet recruitment can be increased for maximal efforts. These results also suggest that neuromuscular adaptations to training require a specific cervical exercise

neck muscles; magnetic resonance imaging

INTRODUCTION

RESISTANCE TRAINING of human limb muscle elicits gains in strength that are greater than increases in muscle size during the initial phase of training (19, 26, 27, 31). This is accompanied by increases in maximal integrated electromyogram (iEMG) and decreases in the slope of the iEMG-force relationship (14, 22, 26). It has also been shown that the absolute area of muscle showing exercise-induced contrast shift in magnetic resonance (MR) images is reduced for a given submaximal load after short-term resistance training (27). These observations suggest that the early increases in strength are the result of neural adaptation, although the exact nature is unclear. Similarly, resistance training of cervical musculature has been shown to evoke increases in strength that are not associated with concomitant increases in muscle size (9). Cervical resistance training has also been shown to increase functional range of motion and to reduce pain and weakness in individuals with neck disorders (4, 16). However, the underlying neuromuscular adaptations to cervical resistance training have received little attention.

MR imaging is frequently used for clinical diagnostic applications because of the detailed visualization of soft tissue that it provides. Recent developments in MR imaging have enabled the acquisition of physiological, or functional, measurements in addition to the more traditional anatomic information. Of particular interest to the study of neuromuscular physiology is the observation that exercise elicits contrast shifts in proton transverse (spin-spin) relaxation times (T2) of skeletal muscle (12). This contrast shift is correlated with iEMG activity (1), increases with exercise intensity (1, 8, 20, 27), and relates to isometric torque with electromyostimulation (2). Exercise-induced increases in T2 have also been shown to be a sensitive marker of muscle activation, with contrast shifts being observed with as few as two repetitions at 80% and five repetitions at 25% of maximum (39). The increase in T2 can be quantified to provide a noninvasive measure of 1) the intensity of recently performed muscular activity, 2) the absolute and relative cross-sectional area (CSA) of muscle used, and 3) the pattern of use among and within individual muscles. Therefore, exercise-induced contrast shifts in MR images seemed to be an ideal approach to study neuromuscular adaptations of the complex cervical region to resistance training. Also, because conventional resistance exercises likely elicit forceful isometric actions of the cervical musculature for stabilization, it is also not known whether a specific cervical exercise is required for neuromuscular adaptations to occur. This would reduce the necessity of performing specific exercises for the cervical musculature if adaptations occur with conventional resistance training. Thus the purpose of this study was to examine cervical neuromuscular adaptations to resistance training, with and without a specific cervical exercise.

METHODS

RESULTS

DISCUSSION

The most notable finding of this study was derecruitment of previously active muscles at a given absolute load after resistance training. In agreement with previous observations (7), six cervical muscles (LS, LSC, SMA, SC, SEC, and SCM) demonstrated a T2 contrast shift after head-extension exercise pretraining. However, after 12 wk of resistance training that included progressive overload head-extension exercise, only three muscles (SC, SEC, and SCM) presented a contrast shift after head-extension exercise at the same absolute load. To our knowledge, this is the first report of derecruitment of previous active muscles during performance of the same movement after resistance training. The ability to recruit the LS, LSC, and SMA was not lost, however, because these muscles demonstrated a comparable contrast shift after maximal exercise posttraining. The derecruitment of the LS, LSC, and SMA, combined with reduced absolute use of the SC, SEC, and SCM, resulted in a 31% decrease in the area of muscle demonstrating a contrast shift to perform exercise at the same load. This is comparable to the 30-40% decrease in the absolute area of the quadriceps femoris demonstrating contrast shift at various submaximal knee-extension loads after 9 wk of resistance training reported by Ploutz et al. (27). The observation that less area of muscle is required to lift the same absolute load after resistance training is also indirectly supported by findings of increased maximal iEMG and a decrease in the slope of the iEMG-force relationship after resistance training (14, 22, 26). This occurred such that EMG was reduced during performance of the same given load after training. However, it should be noted the others have reported no change in iEMG after resistance training (5, 13).

Although the exact biochemical basis of the exercise-induced contrast shift is not known, it is generally accepted that the recruitment of muscle and subsequent metabolic demand are involved. Because resistance training does not cause an appreciable increase in the ability of skeletal muscle to supply energy per unit of contractile machinery (19, 27, 34), the reduced contrast shift is likely the result of neural adaptations. This neural adaptation may involve the desynchronization of motor unit recruitment. Desynchroniztion of motor unit firing has been shown to enhance force development and delay fatigue during submaximal muscle actions (6, 24). This is believed to occur because the "slack" of the passive force-transmitting filaments in muscle is overcome and maintained such that subsequent motor unit activity may contribute to external force development. This seemingly contradicts the one report of increased motor unit synchronization with resistance training (25). However, the increased synchronization was only observed for very short bursts at maximal or near-maximal isometric actions and not during repetitive submaximal actions as used in the present study. It is also possible that the energetic advantage of desynchronized motor unit activity after resistance training contributes indirectly to the derecruitment of cervical muscles. An inherent motor recruitment hierarchy may exist such that the SC, SEC, and SCM muscles are preferentially activated before the LS, LSC, and SMA muscles during head-extension. Desynchronization of the SC, SEC, and SCM muscles and subsequent increased fatigue resistance would likely reduce the necessity of recruiting the LS, LSC, and SMA muscles for completion of the exercise. This would reflect a motor adaptation that optimizes the energetic cost of movement. In this regard, training may also result in preferential use of muscle fibers with low action-myosin adenosinetriphosphatase activity and high oxidative capacity (1). Thus, during times of increased contractile activity, there would be less disturbance of energy balance within the fiber and reduced fatigue susceptibility. Because skeletal muscle T2 increases with cellular energy imbalance (37), this may also account for the reduced contrast shift posttraining.

Although desynchronization of motor unit activity and/or preferential use of fatigue-resistant fibers may contribute to the derecruitment observed in the present study, other potential mechanisms also exist. Voluntary movements are controlled by signals that originate in motor cortex neurons. It is generally believed that there is an inherent motor program that results in a sequential, coordinated firing of specific motoneurons to produce a given movement. It has been shown that skeletal muscles receive input from multiple areas of the motor cortex and that individual cortical neurons have connections to motoneurons that innervate more than one muscle (see Ref. 10). This diffuse pattern of connections may allow cortical neurons to select from the multitude of possible muscle recruitment combinations to produce a specific movement. Thus, with training, the motor program may be modified so that muscle recruitment patterns are altered. Because of the noted anatomic and functional redundancy of cervical muscles (36, 38), this region may be predisposed to such motor program modification in an effort to enhance neuromuscular function.

The proprioceptive system of the cervical region is composed of a diverse population of numerous receptors. Neck muscles contain large numbers of muscle spindles, Golgi tendon organs, pacinian corpuscles, and free nerve endings (29). These receptors serve to provide the central nervous system with detailed information about head position and movement. This sensory information may then be used to aid control of head movement by modifying subsequent descending neural signals. Over time, this modification of sensory-motor integration may be mediated by cerebellar activity (see Ref. 17). The cerebellum has been shown to be critical for coordination of movement (18, 35) and is believed to store muscle activation patterns that are optimized for movement objectives based on sensory information (see Ref. 33). It has been suggested that resistance training alters the sensitivity of muscle receptors (22). One possible consequence may be a disinhibition of protective mechanisms, which would likely allow for greater use of the primary head extensors and reduce the need to recruit other muscles.

Regardless of the mechanism, derecruitment of the LS, LSC, and SMA muscles suggests that they are not preferred head extensors. This is also supported by our previous observations that these muscles demonstrate less contrast shift during high-force head extension than do the SC, SEC, and SCM in untrained individuals (7). A likely consequence of this derecruitment would be an increase in the relative stress placed on the SC, SEC, and SCM during high-force loading. This may, in part, explain the marked (25%) hypertrophy of these muscles in response to head-extension resistance training (9).

The musculoskeletal system of the cervical spine is among the most complex of the human body. Cervical muscles demonstrate marked morphological diversity to permit and control the wide variety of head movements that is possible. Several muscles are pennate to the head-extension movement plane, and thus all of the force developed by these muscles does not contribute directly to the movement. Some evidence from animal studies that used isolated muscle preparations suggests that force prediction is enhanced when pennation angle is considered and the physiological CSA of a muscle is estimated (see Ref. 11). However, the advantage of using physiological CSA to predict functional characteristics has not been demonstrated in vivo. Rutherford and Jones (30) failed to demonstrate a relationship between pennation and force-generating capacity in the human quadriceps, and Scott and Winter (32) reported better muscle force estimation when pennation angle was neglected compared with a model of fixed pennation angle. Estimates of muscle pennation angle and fascicle length are generally based on normative cadaver data, which, to the authors' knowledge, do not exist for all of the human cervical muscles considered in this study. Furthermore, force development in vivo is usually accomplished through the involvement of several muscles acting synergistically (see Ref. 15). This makes the determination of individual muscle contribution to force production uncertain and may partially explain the limitations associated with physiological CSA to predict muscle functional properties in vivo.

Most resistance studies 8-24 wk in duration demonstrate 8-50% increases in strength (see Ref. 23). Comparable strength increases, including the 34% increase in 3 × 10-RM head-extension load observed in the present study, have been reported for specific training of the cervical musculature (4, 16, 28). The initial phase of resistance training also evokes increases in strength that are not associated with concomitant increases in muscle size (27). It is possible that the early gain in strength is a neural adaptation, such as increased muscle activation. The increase in iEMG frequently (14, 22, 26), but not always (5, 13), observed after resistance training supports this contention. The results of the present study also suggest that resistance training increases the ability to activate cervical muscles primarily used in training. Specific training of head extension increased the relative area of the SC, SEC, and SCM, demonstrating an exercise-induced contrast shift at maximal (100%) loads. If resistance training improves muscle activation, it is likely an increase in the ability to recruit high-threshold motor units that are characterized by high twitch force and rapid twitch time (31). Along with the increased strength, the ability to recruit these motor units would likely help prevent or reduce the severity of injury resulting from mechanical trauma by enabling rapid force development to minimize head and cervical displacement. It is not know if the apparent increase in muscle activation is the result of an increased central drive and/or disinhibition of protective mechanisms. Some researchers have also suggested (see Ref. 21) that adaptations within the muscle such as altered fiber type composition, increased fiber pennation angle, increased contractile material packing, and connective tissue attachment may contribute to the early gains in strength that are greater than increases in muscle size. However, these proposed mechanisms have received little experimental support.

In summary, 12 wk of specific cervical resistance training increased head-extension strength by 34% and decreased the CSA of cervical muscle used to perform exercise at the same absolute load by 31%. This decrease involved derecruitment of the LS, LSC, and SMA muscles. The results of the present study suggest functional redundancy of the cervical muscles that can be modified by high-force loading. Although the exact mechanism(s) for this adaptation is unclear, it likely involves an increase in force development or fatigue resistance of primary head extensors (SC, SEC, and SCM) due to desychronization of their use, a reorganization of higher centers that regulate muscle recruitment, and/or altered reflex input to descending neurons innervating cervical musculature. The results also suggest that untrained individuals are unable to maximally activate cervical muscles and that resistance training increases the ability to recruit muscles that are primarily involved with the head movement used in training. To elicit these neuromuscular adaptations, it appears that a specific cervical exercise is required.

ACKNOWLEDGEMENTS

The authors thank the subjects who participated in this study and Dr. Michael Lannoo for helpful comments on the manuscript. They also give special thanks to St. Mary's Hospital (Athens, GA) for use of the MR imager and to Debbie Eliopulos and Lisa Johnson for technical support.

FOOTNOTES

Address for reprint requests: G. A. Dudley, Dept. of Exercise Science, 115F Ramsey Center, The Univ. of Georgia, 300 River Rd., Athens, GA 30602 (E-mail: gdudley@coe.uga).

Received 4 April 1997; accepted in final form 8 August 1997.

REFERENCES